567
Views
0
CrossRef citations to date
0
Altmetric
Special Report

The zebrafish as a potential model for vaccine and adjuvant development

, , , , , , , , , & show all
Pages 535-545 | Received 06 Feb 2024, Accepted 17 Apr 2024, Published online: 09 May 2024

References

  • Hotez PJ, Gilbert S, Saville M, et al. COVID-19 vaccines and the pandemic: lessons learnt for other neglected diseases and future threats. BMJ Glob Health. 2023;8(6):e011883. doi: 10.1136/bmjgh-2023-011883
  • Hogan MJ, Pardi N. mRNA vaccines in the COVID-19 pandemic and beyond. Annu Rev Med. 2022;73(1):17–39. doi: 10.1146/annurev-med-042420-112725
  • Jacob-Dolan C, Barouch DH. COVID-19 Vaccines: Adenoviral Vectors. Annu Rev Med. 2022 Jan 27;73:41–54. doi: 10.1146/annurev-med-012621-102252
  • Hotez PJ, Bottazzi ME. Whole inactivated virus and protein-based COVID-19 vaccines. Annu Rev Med. 2022;73:55–64. doi: 10.1146/annurev-med-042420-113212
  • Hotez PJ. Global vaccine access demands combating both inequity and hesitancy. Health Aff. 2023;42(12):1681–1688. doi: 10.1377/hlthaff.2023.00775
  • Dzau V, Swaminathan S, Baker C, et al. The 100 days mission: how a new medical-countermeasures network can deliver equity and innovation. Lancet. 2023;402(10412):1507–1510. doi: 10.1016/S0140-6736(23)01775-0
  • Lee B, Nanishi E, Levy O, et al. Precision vaccinology approaches for the development of adjuvanted vaccines targeted to distinct vulnerable populations. Pharmaceutics. 2023;15(6):1766. doi: 10.3390/pharmaceutics15061766
  • Casanova JL, Anderson MS. Unlocking life-threatening COVID-19 through two types of inborn errors of type I IFNs. J Clin Invest. 2023;133(3):e166283. doi: 10.1172/JCI166283
  • Black S, Bloom DE, Kaslow DC, et al. Transforming vaccine development. Semin Immunol. 2020;50:101413. doi: 10.1016/j.smim.2020.101413
  • Rappuoli R, De Gregorio E, Del Giudice G, et al. Vaccinology in the post-COVID-19 era. Proc Natl Acad Sci USA. 2021;118(3):e2020368118.
  • Hubrecht RC, Carter E. The 3Rs and humane experimental technique: implementing change. Animals (Basel). 2019;9(10):754. doi: 10.3390/ani9100754
  • Tang B, More V. Recent advances in drug discovery toxicology. Int J Toxicol. 2023;42(6):535–550. doi: 10.1177/10915818231189659
  • Bondue T, Berlingerio SP, van den Heuvel L, et al. The zebrafish embryo as a model organism for testing mRNA-based therapeutics. Int J Mol Sci. 2023;24(13):11224. doi: 10.3390/ijms241311224
  • Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496(7446):498–503. doi: 10.1038/nature12111. Erratum in: Nature. 2014 Jan 9;505(7482):248. Cooper, James [corrected to Cooper, James D]; Eliott, David [corrected to Elliot, David]; Mortimer, Beverly [corrected to Mortimore, Beverley]; Begum, Sharmin [added]; Lloyd, Christine [added]; Lanz, Christa [added]; Raddatz, Günter [added]; Schuster, Ste.
  • Dong W, Akasaka I, Komiyama A, et al. Augmentation of pectoral fin teratogenicity by Thalidomide in human cytochrome P450 3A-Expressing zebrafish. Pharmaceuticals (Basel). 2023;16(3):368. doi: 10.3390/ph16030368
  • Streisinger G, Walker C, Dower N, et al. Production of clones of homozygous diploid zebra fish (brachydanio rerio). Nature. 1981;291(5813):293–296. doi: 10.1038/291293a0
  • Brown K. An interview with Christiane Nüsslein-Volhard. Development. 2017;144(21):3851–3854. doi: 10.1242/dev.159582
  • Zebrafish Core [Internet]. Houston: Baylor College of Medicine; 2024 [cited 2024 Jan 13]. Available from: https://www.bcm.edu/research/atc-core-labs/zebrafish-core.
  • Traver D, Yoder J. Immunology (chapter 19) In: the zebrafish in biomedical research: biology, husbandry, diseases, and research applications. Am Coll Lab Animal Med. Academic Press. 2020. 191–216.
  • Bailone RL, Fukushima HCS, Ventura Fernandes BH, et al. Zebrafish as an alternative animal model in human and animal vaccination research. Lab Anim Res. 2020;36(1):13. doi: 10.1186/s42826-020-00042-4
  • D’Costa A, Shepherd IT. Zebrafish development and genetics: introducing undergraduates to developmental biology and genetics in a large introductory laboratory class. Zebrafish. 2009;6(2):169–177. doi: 10.1089/zeb.2008.0562
  • Lai KP, Gong Z, Tse WKF. Zebrafish as the toxicant screening model: transgenic and omics approaches. Aquat Toxicol. 2021;234:105813. doi: 10.1016/j.aquatox.2021.105813
  • Baranasic D, Hörtenhuber M, Balwierz PJ, et al. Multiomic atlas with functional stratification and developmental dynamics of zebrafish cis-regulatory elements. Nat Genet. 2022;54(7):1037–1050. doi: 10.1038/s41588-022-01089-w
  • Bogdanović O, Fernández-Miñán A, Tena JJ, et al. The developmental epigenomics toolbox: ChIP-seq and MethylCap-seq profiling of early zebrafish embryos. Methods. 2013;62(3):207–215. doi: 10.1016/j.ymeth.2013.04.011
  • Link V, Shevchenko A, Heisenberg CP. Proteomics of early zebrafish embryos. BMC Dev Biol. 2006;6:1. doi: 10.1186/1471-213X-6-1
  • Harvey SA, Sealy I, Kettleborough R, et al. Identification of the zebrafish maternal and paternal transcriptomes. Development. 2013;140(13):2703–2710. doi: 10.1242/dev.095091
  • Spanjaard B, Hu B, Mitic N, et al. Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nat Biotechnol. 2018;36(5):469–473.
  • Farrell JA, Wang Y, Riesenfeld SJ, et al. Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis. Science. 2018;360(6392):eaar3131. doi: 10.1126/science.aar3131
  • Farnsworth DR, Saunders LM, Miller AC. A single-cell transcriptome atlas for zebrafish development. Dev Biol. 2020;459(2):100–108. doi: 10.1016/j.ydbio.2019.11.008
  • Saunders LM, Srivatsan SR, Duran M, et al. Embryo-scale reverse genetics at single-cell resolution. Nature. 2023;623(7988):782–791. doi: 10.1038/s41586-023-06720-2
  • Lange M, Granados A, VijayKumar S, et al. Zebrahub – multimodal zebrafish developmental atlas reveals the state-transition dynamics of late-vertebrate pluripotent axial progenitors. bioRxiv. 2023.03.06.531398. doi: 10.1101/2023.03.06.531398
  • Zebrahub [Internet]. San Francisco: Chan Zuckerberg Biohub; 2024 [cited 2024 Jan 13]. Available from: https://zebrahub.ds.czbiohub.org/.
  • Bambino K, Chu J. Zebrafish in toxicology and environmental health. Curr Top Dev Biol. 2017;124:331–367. doi: 10.1016/bs.ctdb.2016.10.007
  • Miyawaki I. Application of zebrafish to safety evaluation in drug discovery. J Toxicol Pathol. 2020;33(4):197–210. doi: 10.1293/tox.2020-0021
  • Organisation of Economic Cooperation and Development (OECD). Test No. 236: fish embryo acute toxicity (FET) test, OECD guidelines for the testing of chemicals, section 2, 2013. Paris: OECD Publishing; [cited Jan 7, 2024]. doi: 10.1787/9789264203709-en
  • Prior H, Haworth R, Labram B, et al. Justification for species selection for pharmaceutical toxicity studies. Toxicol Res (Camb). 2020;9(6):758–770.
  • Prior H, Baldrick P, Beken S, et al. Opportunities for use of one species for longer-term toxicology testing during drug development: a cross-industry evaluation. Regul Toxicol Pharmacol. 2020;113:104624. doi: 10.1016/j.yrtph.2020.104624
  • Guo M, Xiong M, Peng J, et al. Multi-omics for COVID-19: driving development of therapeutics and vaccines. Natl Sci Rev. 2023;10(9):nwad161. doi: 10.1093/nsr/nwad161
  • Parab A, Kumar Bhatt L, Omri A. Targeting epigenetic mechanisms: a boon for cancer immunotherapy. Biomedicines. 2023;11(1):169. doi: 10.3390/biomedicines11010169
  • Sopel N, Müller-Deile J. The zebrafish model to understand epigenetics in renal diseases. Int J Mol Sci. 2021;22(17):9152. doi: 10.3390/ijms22179152
  • Ping S, Lin W, Ming R, et al. Toxic effects of four cardiovascular drugs on the development and epigenetics of zebrafish (danio rerio). Sci Total Environ. 2022;846:157360. doi: 10.1016/j.scitotenv.2022.157360
  • Wang S, Bryan C, Xie J, et al. Atrazine exposure in zebrafish induces aberrant genome-wide methylation. Neurotoxicol Teratol. 2022;92:107091. doi: 10.1016/j.ntt.2022.107091
  • Akemann C, Meyer DN, Gurdziel K, et al. TCDD-induced multi- and transgenerational changes in the methylome of male zebrafish gonads. Environ Epigenet. 2020;6(1):dvaa010. doi: 10.1093/eep/dvaa010
  • Falisse E, Ducos B, Stockwell PA, et al. DNA methylation and gene expression alterations in zebrafish early-life stages exposed to the antibacterial agent triclosan. Environ Pollut. 2018;243(Pt B):1867–1877. doi: 10.1016/j.envpol.2018.10.004
  • Aluru N. Epigenetic effects of environmental chemicals: insights from zebrafish. Curr Opin Toxicol. 2017;6:26–33. doi: 10.1016/j.cotox.2017.07.004
  • Terrazas-Salgado L, García-Gasca A, Betancourt-Lozano M, et al. Epigenetic transgenerational modifications induced by xenobiotic exposure in zebrafish. Front Cell Dev Biol. 2022;10:832982. doi: 10.3389/fcell.2022.832982
  • US. National institutes of health office of laboratory animal welfare. Zebrafish; [cited 2023 Dec 24]. Available from: https://olaw.nih.gov/policies-laws/21st-century-cures-act/Zebrafish
  • Xu B, Pu M, Jiang K, et al. Maternal or paternal antibiotics? Intergenerational transmission and reproductive toxicity in zebrafish. Environ Sci Technol. 2023 Dec 19. doi: 10.1021/acs.est.3c06090. Epub ahead of print. PMID: 38113251.
  • Stebbings R, Maguire S, Armour G, et al. Developmental and reproductive safety of AZD1222 (ChAdox1 nCoV-19) in mice. Reprod Toxicol. 2021;104:134–142. doi: 10.1016/j.reprotox.2021.07.010
  • Ackley D, Birkebak J, Blumel J, et al. FDA and industry collaboration: identifying opportunities to further reduce reliance on nonhuman primates for nonclinical safety evaluations. Regul Toxicol Pharmacol. 2023;138:105327. doi: 10.1016/j.yrtph.2022.105327
  • Ye M, Chen Y. Zebrafish as an emerging model to study gonad development. Comput Struct Biotechnol J. 2020;18:2373–2380. doi: 10.1016/j.csbj.2020.08.025
  • Dranow DB, Hu K, Bird AM, et al. Bmp15 is an oocyte-produced signal required for maintenance of the adult female sexual phenotype in zebrafish. PloS Genet. 2016;12(9):e1006323. doi: 10.1371/journal.pgen.1006323
  • Wilson CA, Batzel P, Postlethwait JH. Direct male development in chromosomally ZZ zebrafish. Front Cell Dev Biol. 2024;12. doi: 10.1101/2023.12.27.573483
  • Rajesh V, Divya PK. Embryonic exposure to decitabine induces multiple neural tube defects in developing zebrafish. Fish Physiol Biochem. 2023;49(6):1357–1379. doi: 10.1007/s10695-023-01261-x Epub ahead of print.
  • Valdivieso A, Caballero-Huertas M, Moraleda-Prados J, et al. Exploring the effects of rearing densities on epigenetic modifications in the zebrafish gonads. Int J Mol Sci. 2023;24(21):16002. doi: 10.3390/ijms242116002
  • MacGowan J, Cardenas M, Williams MK. Vangl2 deficient zebrafish exhibit hallmarks of neural tube closure defects. bioRxiv [Preprint]. 2023. doi:10.1101/2023.11.09.566412. PMID: 37986956; PMCID: PMC10659374.
  • de Andrade Belo MA, Charlie-Silva I. Teleost fish as an experimental model for vaccine development. Methods Mol Biol. 2022;2411:175–194. doi: 10.1007/978-1-0716-1888-2_10
  • Sullivan C, Soos BL, Millard PJ, et al. Modeling virus-induced inflammation in zebrafish: a balance between infection control and excessive inflammation. Front Immunol. 2021;12:636623. doi: 10.3389/fimmu.2021.636623
  • Martínez-López A, Tyrkalska SD, Alcaraz-Pérez F, et al. Evolution of LPS recognition and signaling: the bony fish perspective. Dev Comp Immunol. 2023 Aug;145:104710. doi: 10.1016/j.dci.2023.104710. Epub 2023 Apr 18. PMID: 37080369.
  • Weber ANR. Fish TLR5 develops a taste for viral RNA. EMBO Rep. 2022;23(8):e55443. doi: 10.15252/embr.202255443
  • Mosaheb MM, Reiser ML, Wetzler LM. Toll-like receptor ligand-based vaccine adjuvants require intact MyD88 signaling in antigen-presenting cells for germinal center formation and antibody production. Front Immunol. 2017;8:225. doi: 10.3389/fimmu.2017.00225
  • Marty-Roix R, Vladimer GI, Pouliot K, et al. Identification of QS-21 as an inflammasome-activating molecular component of saponin adjuvants. J Biol Chem. 2016;291(3):1123–1136. doi: 10.1074/jbc.M115.683011
  • Zhu W, Dong C, Wei L, et al. Promising adjuvants and platforms for influenza vaccine development. Pharmaceutics. 2021;13(1):68. doi: 10.3390/pharmaceutics13010068
  • Chang MX, Xiong F, Wu XM, et al. The expanding and function of NLRC3 or NLRC3-like in teleost fish: recent advances and novel insights. Dev Comp Immunol. 2021 Jan;114:103859. doi: 10.1016/j.dci.2020.103859
  • Slezak A, Chang K, Hossainy S, et al. Therapeutic synthetic and natural materials for immunoengineering. Chem Soc Rev. 2024 Jan 3;53(4):1789–1822. doi:10.1039/d3cs00805c. Epub ahead of print.
  • Haynes BF, Corey L, Fernandes P, et al. Prospects for a safe COVID-19 vaccine. Sci Transl Med. 2020;12(568):eabe0948. doi: 10.1126/scitranslmed.abe0948
  • Flynn JL. Lessons from experimental mycobacterium tuberculosis infections. Microbes Infect. 2006;8(4):1179–1188. doi: 10.1016/j.micinf.2005.10.033
  • Swaim LE, Connolly LE, Volkman HE, et al. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun. 2006;74(11):6108–6117. doi: 10.1128/IAI.00887-06. Erratum in: Infect Immun. 2007 Mar;75(3):1540.
  • Cambier CJ, Takaki KK, Larson RP, et al. Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature. 2014;505(7482):218–222. doi: 10.1038/nature12799
  • Liu Z, Ulrich vonBargen R, Kendricks AL, et al. Localized cardiac small molecule trajectories and persistent chemical sequelae in experimental chagas disease. Nat Commun. 2023;14(1):6769. doi: 10.1038/s41467-023-42247-w. PMID: 37880260.
  • Gomes MC, Brokatzky D, Bielecka MK, et al. Shigella induces epigenetic reprogramming of zebrafish neutrophils. Sci Adv. 2023;9(36):eadf9706. doi: 10.1126/sciadv.adf9706
  • Renshaw SA, Trede NS. A model 450 million years in the making: zebrafish and vertebrate immunity. Dis Model Mech. 2012;5(1):38–47. doi: 10.1242/dmm.007138
  • Tyrkalska SD, Martínez-López A, Arroyo AB, et al. Differential proinflammatory activities of spike proteins of SARS-CoV-2 variants of concern. Sci Adv. 2022;8(37):eabo0732. doi: 10.1126/sciadv.abo0732 Erratum in: Sci Adv. 2022 Dec 23;8(51):eadf9695.
  • Wang Z, You X, Zhang Y, et al. Poly(I: C) induces anti-inflammatory response against secondary LPS challenge in zebrafish larvae. Fish Shellfish Immunol. 2023;144:109285. doi: 10.1016/j.fsi.2023.109285. Epub ahead of print. PMID: 38092095.
  • Coccia M, Collignon C, Hervé C, et al. Cellular and molecular synergy in AS01-adjuvanted vaccines results in an early IFNγ response promoting vaccine immunogenicity. NPJ Vaccin. 2017 Sep;2(1):25. doi: 10.1038/s41541-017-0027-3 Erratum in: NPJ Vaccines. 2018;3:13.
  • Hotez PJ, Adhikari R, Chen WH, et al. From concept to delivery: a yeast-expressed recombinant protein-based COVID-19 vaccine technology suitable for global access. Expert Rev Vaccines. 2023;22(1):495–500. doi: 10.1080/14760584.2023.2217917
  • Myllymäki H, Niskanen M, Luukinen H, et al. Identification of protective postexposure mycobacterial vaccine antigens using an immunosuppression-based reactivation model in the zebrafish. Dis Model Mech. 2018;11(3):dmm033175. doi: 10.1242/dmm.033175
  • Onoja A, von Gerichten J, Lewis HM, et al. Meta-analysis of COVID-19 metabolomics identifies variations in robustness of biomarkers. Int J Mol Sci. 2023;24(18):14371. doi: 10.3390/ijms241814371
  • Hu YL, Xiang LX, Shao JZ. Identification and characterization of a novel immunoglobulin Z isotype in zebrafish: implications for a distinct B cell receptor in lower vertebrates. Mol Immunol. 2010;47(4):738–746. doi: 10.1016/j.molimm.2009.10.010
  • Dornburg A, Ota T, Criscitiello MF, et al. From IgZ to IgT: a call for a common nomenclature for immunoglobulin heavy chain genes of ray-finned fish. Zebrafish. 2021;18(6):343–345. doi: 10.1089/zeb.2021.0071
  • Zimmerman AM, Moustafa FM, Romanowski KE, et al. Zebrafish immunoglobulin IgD: unusual exon usage and quantitative expression profiles with IgM and IgZ/T heavy chain isotypes. Mol Immunol. 2011;48(15–16):2220–2223. doi: 10.1016/j.molimm.2011.06.441
  • Jørgensen LVG, Korbut R, Jeberg S, et al. Association between adaptive immunity and neutrophil dynamics in zebrafish (danio rerio) infected by a parasitic ciliate. PLOS ONE. 2018;13(9):e0203297. doi: 10.1371/journal.pone.0203297
  • Ji JF, Hu CB, Shao T, et al. Differential immune responses of immunoglobulin Z subclass members in antibacterial immunity in a zebrafish model. Immunology. 2021;162(1):105–120. doi: 10.1111/imm.13269
  • Pedroso GL, Hammes TO, Escobar TD, et al. Blood collection for biochemical analysis in adult zebrafish. J Vis Exp. 2012 63;(63):e3865. doi: 10.3791/3865
  • Castro R, Jouneau L, Pham HP, et al. Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection. PLOS Pathog. 2013;9(1):e1003098. doi: 10.1371/journal.ppat.1003098
  • Chen WH, Du L, Chag SM, et al. Yeast-expressed recombinant protein of the receptor-binding domain in SARS-CoV spike protein with deglycosylated forms as a SARS vaccine candidate. Hum Vaccin Immunother. 2014;10(3):648–658. doi: 10.4161/hv.27464
  • Chen WH, Chag SM, Poongavanam MV, et al. Optimization of the production process and characterization of the yeast-expressed SARS-CoV recombinant receptor-binding domain (RBD219-N1), a SARS vaccine candidate. J Pharm Sci. 2017;106(8):1961–1970. doi: 10.1016/j.xphs.2017.04.037
  • Nyon MP, Du L, Tseng CK, et al. Engineering a stable CHO cell line for the expression of a MERS-coronavirus vaccine antigen. Vaccine. 2018 [Epub 2018 Feb 26];36(14):1853–1862. doi: 10.1016/j.vaccine.2018.02.065
  • Chen WH, Hotez PJ, Bottazzi ME. Potential for developing a SARS-CoV receptor-binding domain (RBD) recombinant protein as a heterologous human vaccine against coronavirus infectious disease (COVID)-19. Hum Vaccin Immunother. 2020;16(6):1239–1242. doi: 10.1080/21645515.2020.1740560
  • Chen WH, Wei J, Kundu RT, et al. Genetic modification to design a stable yeast-expressed recombinant SARS-CoV-2 receptor binding domain as a COVID-19 vaccine candidate. Biochim Biophys Acta Gen Subj. 2021;1865(6):129894. doi: 10.1016/j.bbagen.2021.129893
  • Pollet J, Chen WH, Versteeg L, et al. SARSCoV-2 RBD219-N1C1: a yeast-expressed SARS-CoV-2 recombinant receptor-binding domain candidate vaccine stimulates virus neutralizing antibodies and T-cell immunity in mice. Hum Vaccin Immunother. 2021;17(8):2356–2366.
  • Lee J, Liu Z, Chen WH, et al. Process development and scale-up optimization of the SARS-CoV-2 receptor binding domain-based vaccine candidate, RBD219-N1C1. Appl Microbiol Biotechnol. 2021;105(10):4153–4165.
  • Pollet J, Strych U, Chen WH, et al. Receptor-binding domain recombinant protein on alum-CpG induces broad protection against SARS-CoV-2 variants of concern. bioRxiv [Preprint]. doi:10.1101/2021.07.06.451353 2022:2021.07.06.451353. Update in: Vaccine. 2022 May 8.
  • Chen WH, Tao X, Agrawal AS, et al. Yeast-expressed SARS-CoV recombinant receptor-binding domain (RBD219-N1) formulated with aluminum hydroxide induces protective immunity and reduces immune enhancement. Vaccine. 2020;38(47):7533–7541. doi: 10.1016/j.vaccine.2020.09.061
  • Pino M, Abid T, Pereira Ribeiro S, et al. A yeast expressed RBD-based SARS-CoV-2 vaccine formulated with 3M-052-alum adjuvant promotes protective efficacy in non-human primates. Sci Immunol. 2021;6(61):eabh3634.
  • Chen WH, Pollet J, Strych U, et al. Yeast-expressed recombinant SARS-CoV-2 receptor binding domain RBD203-N1 as a COVID-19 protein vaccine candidate. Protein Expr Purif. 2022;190:106003. doi: 10.1016/j.pep.2021.106003
  • Thimmiraju SR, Adhikari R, Villar MJ, et al. A recombinant protein XBB.1.5 RBD/Alum/CpG vaccine elicits high neutralizing antibody titers against omicron subvariants of SARS-CoV-2. Vaccines (Basel). 2023;11(10):1557. doi: 10.3390/vaccines11101557
  • Choi SSA, Chan HH, Chan CM, et al. Neuromasts and olfactory organs of zebrafish larvae represent possible sites of SARS-CoV-2 pseudovirus host cell entry. J Virol. 2022;96(24):e0141822. doi: 10.1128/jvi.01418-22
  • Tyrkalska SD, Candel S, Pedoto A, et al. Zebrafish models of COVID-19. FEMS Microbiol Rev. 2023;47(1):fuac042. doi: 10.1093/femsre/fuac042
  • Tyrkalska SD, Martínez-López A, Pedoto A, et al. The spike protein of SARS-CoV-2 signals via Tlr2 in zebrafish. Dev Comp Immunol. 2023;140:104626. doi: 10.1016/j.dci.2022.104626
  • Bastos TSB, de Paula AGP, Dos Santos Luz RB, et al. A novel insight on SARS-CoV-2 S-derived fragments in the control of the host immunity. Sci Rep. 2023;13(1):8060. doi: 10.1038/s41598-023-29588-8 Erratum in: Sci Rep. 2023 Jul 25;13(1):12012.
  • Ventura Fernandes BH, Feitosa NM, Barbosa AP, et al. Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: a tool to study its hazardous for human health? Sci Total Environ. 2022;813:152345. doi: 10.1016/j.scitotenv.2021.152345
  • Hotez PJ. Preventing the next pandemic: vaccine diplomacy in a time of anti-science. Baltimore, MD: Johns Hopkins University Press; 2021.
  • Raeven RHM, van Riet E, Meiring HD, et al. Systems vaccinology and big data in the vaccine development chain. Immunology. 2019;156(1):33–46. doi: 10.1111/imm.13012
  • Masud S, Torraca V, Meijer AH. Modeling infectious diseases in the context of a developing immune system. Curr Top Dev Biol. 2017;124:277–329. doi: 10.1016/bs.ctdb.2016.10.006